Mangroves are shrubs and trees which grow on sea and estuarine shores between the mid-tide level and the extreme high tide mark. The soils in which they grow are usually grey in colour, poorly drained, rich in organic matter and anoxic. The soil water is always saline to some degree and usually smells strongly of sulphide compounds. The greater part of the shore area potentially occupied by mangroves is regularly flooded by the tide to a depth of up to half the total tidal range and the soil surface covered by water for up to six hours.
All mangroves show the development of specialised structures which facilitate the entry of oxygen into the root system. The extent of these structures varies from the simple knob-like protuberances which arise from the roots of Aegiceras corniculatum to the spectacular looping root system of Rhizophora stylosa and the giant woody pneumatophores of Sonneratia alba. Mangrove root systems can be very extensive. As an example, on Towra Point in Botany Bay in Sydney, live Avicennia marina pneumatophores have be found up to 30 metres from the base of the nearest tree of a stand even though none of the trees exceed 4 metres in height.
It is clear that one of the essential problems which a plant must solve before it can grow in such an environment is the supply of oxygen to its root system in sufficient quantity to enable root growth and efficient metabolic activity. The vast majority of land plants obtain sufficient oxygen for root growth and activity from the air, via the gas spaces within the soil, but it is clear that the anoxic nature of 'mangrove' soils makes this supply route impossible for these plants. Mangroves have solved this problem by the development of internal gas transport pathways extending throughout the entire root system and communicating with the air by means of lenticels or other specialised water excluding structures. The supply of oxygen to mangrove root systems is further complicated by the tide which partially or completely isolates the root system from the air once or twice a day for periods of up to six hours.
1. Do the above ground portions of the root system have sufficient transport capacity to supply the oxygen consumed by the respiration of the root system either by gaseous diffusion or by some 'active' means?
2. Can aerobic respiration be maintained in the root tissue during the period when the system is isolated from the air by the rising tide?
All mangroves appear to have extensive aerenchyma tissue in their root systems and all the published data indicate that the gas spaces contain significant quantities of oxygen. Although mangrove root systems are normally isolated from the air for up to six hours by each tide, no published data indicates an approach to anaerobiosis in the aerenchyma, even following artificial lengthening of tidal cover for up to twenty four hours (e.g. Scholander et al., 1955, Anderson & Kristensen, 1988, Skelton & Allaway, 1996). This implies storage of sufficient oxygen in the gas spaces of the aerenchyma to maintain aerobic conditions within the root irrespective of the state of the tide.
In young plants of Avicennia marina, it has been possible to measure the total capacity of pneumatophores to supply oxygen to the root system by diffusion, the rate at which oxygen is consumed by the roots and the volume of gas spaces within the roots (Curran et al., 1985). These data enable the comparison of the ability of the plant to supply oxygen to its root system and compare this with the root system's demand for oxygen. In this plant it is possible to conclude that the pneumatophores can easily supply sufficient oxygen to maintain aerobic respiration by simple diffusion and that there is sufficient oxygen stored in the root gas spaces when the pneumatophores are first covered by the rising tide to maintain aerobic conditions until they are uncovered by the falling tide.
It is also possible to predict, by calculation, the way in which the oxygen content of the root will change with the state of the tide and these predictions appear consistent with oxygen concentrations measured in situ in different portions of an intact root system.
Modelling of the oxygen concentration changes is complicated by the drop in pressure observed within the root gas spaces while the root system is covered by the tide. This pressure drop (of up to 5 KPa) appears to be related to the observation that the respiratory quotient of isolated root tissue is less than 1.0 and often between 0.8 and 0.9, but it is unlikely that the gas inflow caused by the release of this pressure differential is a significant factor in the aeration of the roots of Avicennia marina.
For a mangrove plant to establish itself, the seed and seedling must be able to survive in the position which the adult plant will occupy, but it must do this prior to the development of the specialised anatomical adaptations for root ventilation so noticeable in the mature plants.
In Avicennia marina, pneumatophores rarely develop before the seedlings are one year old. Not only does the developing root system lack the direct access to the atmosphere provided by pneumatophores, but the entire plant may be totally submerged for a significant portion of each day during which time gas exchange with the atmosphere is not possible. As the seedling grows there is extensive development of aerenchyma which can be shown to form a continuum of gas spaces throughout the plant from the spongy mesophyll of the leaf, through the petiole, stem, hypocotyl and into the root (Ashford & Allaway, 1995). While the plant is small, this continuum provides the possibility of transfer of photosynthetic oxygen from leaves to roots and of respiratory carbon dioxide to the leaves when the plant is isolated from the air by the rising tide. The early development of large adventitious roots containing gas spaces which occupy up to 70% of their volume permit storage of oxygen. When the plant is exposed all of these gas spaces communicate with the air through lenticels developed on the stem and hypocotyl.
The initial growth and development of Avicennia marina seedlings appears to be little affected by depth and length of tidal inundation in the first year, except in conditions which are well beyond those under which the plant is normally found. Experiments under simulated tidal conditions indicate that growth is greatest where the period of inundation is between 2 and 7 hours per tidal cycle but the ratio of root dry weight to gas space volume, which would determine the ability of these plants to maintain aerobic respiration at an undiminished rate during tidal cover, did not vary and implied that these systems would remain aerobic for 3.5 hours after tidal cover (Hovenden et al., 1995).
It would appear that the initial development of this mangrove is 'pre-programmed' to take account of the predictable nature of its environment. The 'adaptation' of the root system to its position in the tidal range seems to take place in its next phase of growth when pneumatophores are first developed.
Andersen F. O, Kirstensen E. 1988. Oxygen microgradients in the rhizosphere of the mangrove Avicennia marina. Mar. Ecol. Prog. Ser. 44: 201-204.
Ashford A. E, Allaway W. G. 1995. There is a continuum of gas space in young plants of Avicennia marina. Hydrobiologia 295: 5-11.
Curran M, Cole M, Allaway W. G. 1986. Root aeration and respiration in young mangrove plants (Avicennia marina (Forsk.) Vierh.). Journal of Experimental Botany 37: 1225-1233.
Hovenden M. J, Curran M, Cole M. A, Goulter P. F. E, Skelton N. J, Allaway W. G. 1995. Ventilation and respiration in one-year-old seedlings of grey mangrove Avicennia marina (Forsk.) Vierh. Hydrobiologia 295: 23-29.
Scholander, P. F, Dam, L. van, Scholander, S. I. 1955. Gas exchange in the roots of mangroves. Am. J. Bot. 42, 92-98.
Skelton N. J, Allaway W. G. 1996. Oxygen and pressure changes measured in situ during flooding in roots of the Grey Mangrove Avicennia marina (Forssk.) Vierh. Aquat.Bot. 54:165-175.
Allaway, W. G., Curran, M, Hollington, L. M., Ricketts, M. C., and Skelton, N. J. 2001. Gas space and oxygen exchange in roots of Avicennia marina (Forssk.) Vierh. var. australasica (Walp.) Moldenke ex N. C. Duke, the Grey Mangrove. Wetlands Ecology and Management 9: 211-218.